Phage-plasmids promote recombination and emergence of phages and plasmids

Abstract

Phages and plasmids are regarded as distinct types of mobile genetic elements that drive bacterial evolution by horizontal gene transfer. However, the distinction between both types is blurred by the existence of elements known as prophage-plasmids or phage-plasmids, which transfer horizontally between cells as viruses and vertically within cellular lineages as plasmids. Here, we study gene flow between the three types of elements. We show that the gene repertoire of phage-plasmids overlaps with those of phages and plasmids. By tracking recent recombination events, we find that phage-plasmids exchange genes more frequently with plasmids than with phages, and that direct gene exchange between plasmids and phages is less frequent in comparison. The results suggest that phage-plasmids can mediate gene flow between plasmids and phages, including exchange of mobile element core functions, defense systems, and antibiotic resistance. Moreover, a combination of gene transfer and gene inactivation may result in the conversion of elements. For example, gene loss turns P1-like phage-plasmids into integrative prophages or into plasmids (that are no longer phages). Remarkably, some of the latter have acquired conjugation-related functions to became mobilisable by conjugation. Thus, our work indicates that phage-plasmids can play a key role in the transfer of genes across mobile elements within their hosts, and can act as intermediates in the conversion of one type of element into another.

Analysis and culturing of the prototypic crAssphage reveals a phage-plasmid lifestyle

“…In fact, transposable elements have been shown to frequently jump between PPs and plasmids 83 . These transposition events can catalyze the transition of one element type to another (plasmid to PP, PP to plasmid, PP to integrative phage, etc.)…”

“…These transposition events can catalyze the transition of one element type to another (plasmid to PP, PP to plasmid, PP to integrative phage, etc.) 83 . This raises a series of interesting questions that remain unexplored; how often are these transitions occurring?…”

“…The fact that C. communis does not plaque readily and in liquid culture does not seem to induce a growth defect in its host may suggest that it is in the process of losing its phage functions or that it maintains incredibly strict control over its lytic “on switch.” It is thought that PPs can lose their phage functions altogether once they obtain mobilization genes and an origin of transfer as an alternative method of horizontal transfer 83 . This could simply be due to genetic drift and pseudogenization of phage genes, or more likely due to the fact that PP genomes are larger than those of integrative phages and larger genome size leads to reduced efficiency of genome packaging into phage particles and a single large genetic acquisition event may inhibit packaging altogether 22,84 .…”

“…PPs are also less drastically impacted by disruption of essential genes for one genetic program (phage or plasmid) because the alternate program may remain intact. In fact, transposable elements have been shown to frequently jump between PPs and plasmids 83 . These transposition events can catalyze the transition of one element type to another (plasmid to PP, PP to plasmid, PP to integrative phage, etc.)…”

Specificities and commonalities of the Planctomycetes plasmidome

“…Precisely in the most divergent planctomycetal plasmid, pPLIM01 of Planctopirus limnophila, an essential gene, encoding a protein of unknown function (WP_013112526.1) was recently identified by transposon-directed insertion site sequencing (Rivas-Marin et al, 2023). This plasmid is enriched in phage-related genes and could thus be a phage-plasmid (Pfeifer & Rocha, 2024).…”